Introduction

The issue of spatial–temporal structure in the zooplankton community inhabiting the Omani shelf was basically skipped by basin-scaled International expeditions devoted to the Arabian Sea. For instance, a major part of JGOFS oceanographic stations of 1990s was oriented toward the pelagic processes in oceanic regions (Smith 2005). The earliest expedition that covered coastal Oman, was carried out by R/V “Fridtjof Nansen,” from March to June 1976 and dealt with zooplankton studies (Anonymous 1975). From December 1989 to November 1990, a zooplankton survey of the Omani shelf was carried out by R/V “Rastrelliger,” focusing on the assessment of spatial–temporal variations of total zooplankton biomass (Thangaraja et al. 2011). Later on in August 1995, the US R/V “Malcolm Baldrige” made a part of its sampling along the Omani shelf, with an accent on acoustical measurements of diel vertical migrations (Hitchcock et al. 2002). In 2002, the R/V “Charles Darwin” carried out a 28-day cruise along the Omani shelf, with the main objective of producing a bathymetry map and sampling the benthic community (Jacobs 2003). The survey was accompanied by CTD casts which were important for further insights into the thermo-haline structure of water masses.

A comprehensive study of zooplankton ecology is of great importance for analyzing the states of the northern Indian Ocean like Oman, because many commercial fish species are planktivorous; a challenge which points out the necessity of studying the details of their food resources. An academic interest in zooplankton research is associated in part with seasonal changes, in particular with the phenomenon entitled the “paradox” of the Arabian Sea zooplankton, stating that biomass is invariant despite seasonally changing primary production (Baars 1999; Madhupratap et al. 1996). Magnitudes of seasonal changes in zooplankton biomass are valuable characteristics in understanding the limitation of algal bloom magnitudes by zooplankton grazing (Smith 2001). It is believed that about 40 % of primary production could be ingested by mesozooplankton, which is an indicative of the importance of this group in trophic relationships in epipelagic plankton communities (Roman et al. 2000).

The Omani shelf is the region notorious for its intensive seasonal upwelling, which is footprinted in ontogenetic vertical migrations of abundant zooplankton species. The copepod Calanoides carinatus s.f. is one of these. It has been shown that the population migrates to the upper layers rich in diatoms which it grazes on. However, the data establishing this concept came from a single local sampling site (Smith et al. 1998). In fact, the Oman shelf area was largely missed in all the JGOFS sampling. Schemes of standard transect of the JGOFS cruises point out only one station out of eight, located on the shelf (Lane et al. 1998). In order to estimate the spatial scale of the ontogenetic migration phenomenon, a field survey of the whole shelf is inevitable.

Here we present results of five seasonal surveys carried out over the Omani shelf overlooking the western Arabian Sea. Data come from the expedition sponsored by the Oman Ministry of Fisheries and implemented in 2007–2008 by New Zealand Consultant Bruce Shallard and Associates who subcontracted the New Zealand Institute of Water and Atmospheric Research, Deliotte New Zealand, Independent Fisheries New Zealand, and Al Riyami Group (McKoy et al. 2009). We discuss spatial distribution and seasonal changes in the abundance of species, as well as the total zooplankton biomass.

Data and methods

Data on the wind speed were retrieved from the NCAR/NCEP reanalysis database (Kistler et al. 2001), in which the daily averages were extracted for the western Arabian Sea region incorporating the Omani shelf (15–23°N; 57–60°E). Maps for sea surface height anomalies were acquired from the CCAR Global Near Real-Time SSH Anomaly/Ocean Color Data Viewer (http://eddy.colorado.edu/ccar/data_viewer/index).

Satellite-derived MODIS Aqua weekly Level-3 products for the chlorophyll-a concentration (with a 4-km spatial resolution) were obtained from the National Aeronautics and Space Administration (NASA) database (http://gdata1.sci.gsfc.nasa.gov/daac-bin/G3/gui.cgi?instance_id=ocean_8day). Monthly time series were acquired using the GES-DISC Interactive Online Visualization and Analysis Infrastructure software, as part of the NASA’s Goddard Earth Sciences Data and Information Services Center.

Zooplankton sampling was a part of seasonal surveys consisting of five voyages of the R/V “Mustaqila1” carried out along the shelf in the 20–250 m depth range, from the Ras al Hadd region to the southernmost part of the Omani shelf (to the Yemen border). Sampling was accompanied by the RBD CTD probe casts (with conductivity, temperature, density, and dissolved oxygen concentration measurements), echo-soundings, and fish trawls (Table 1).

Table 1 General characteristics of the “Mustaqila1” voyages
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Zooplankton were collected around the clock at 216 stations along the offshore transects (Fig. 1). A net with an opening of 60 cm equipped with 500 µm mesh net was used for oblique vertical hauls. Samples were preserved in 4 % buffered formaldehyde. The wet weight (mass) of 216 samples was estimated in the lab by using an electronic balance, after blotting, and expressed in mg m−3. Subsamples from 20 samples collected during winter, spring, and summer seasons were subjected to taxonomic analysis to the species level and size measurements.

Fig. 1
figure 1

Zooplankton sampling sites along the Omani shelf from September 2007 to September 2008

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A Simrad EK60 acoustic instrument with 38, 120, and 200 kHz transducers was used for routine acoustic surveys. Transects across the shelf began at a 200 m depth and extended out to 8 km offshore. When deep-scattering layers were identified on the sounder, pelagic trawls were used to catch the organisms. Later on, catches were sorted by species (McKoy et al. 2009). The P55 midwater trawl with a 10 mm liner in the cod end was used to sample mesopelagic organisms.

Results

In terms of time span, a major part of the zooplankton sampling was carried out from January to September 2008. We begin the analysis of seasonal changes from the Winter North-east Monsoon, through the Spring Inter-monsoon and finally, to the Summer South-west Monsoon period. During winter and summer monsoons, the prevailing wind direction is parallel to the coast, but it has opposite directions (Böhm et al. 1999). This does not allow a coastal current (the East Arabian Current) to set up upwelling during winter, but maximizes the offshore Ekman transport and thus the upwelling intensity during the summer.

The year 2008 was notorious for its unusually calm winter monsoon, in which the wind speed in February was gradually decreasing, compared to the previous years, whereas the winds featured in the South-west Monsoon (in August) were gradually increasing (Fig. 2). Overall, summer winds possessed high meridional speeds compared to the winter monsoon winds.

Fig. 2
figure 2

Monthly changes of meridional component of the wind speed over the western Arabian Sea including the Omani shelf region (15–23°N; 57–60°E). Values are positive when the wind blows from west to east

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The series of CTD casts carried out during zooplankton sampling have captured the seasonal variability of the thermo-haline structure over the Omani shelf (Fig. 3).

Fig. 3
figure 3

Vertical distribution of temperature and salinity over the Omani shelf during North-east Monsoon, Spring Inter-monsoon, and South-west Monsoon. Upper panel St.316, 18 February, 2008; 10°01.73°N, 57°21.09°E. Middle panel St.210, 6 May, 2008; 19°11.92°N, 58°08.82°E, and low panel St.173, 18 August, 2008; 18°19.78°N, 57°33.43°E

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This variability is largely based on a reversing of the East Arabian Current, changing its direction from north-eastward during the South-west Monsoon to the opposite (south-westward) during the North-east Monsoon. Figure 3 exemplifies vertical structure corresponding with the monsoonal and inter-monsoonal seasons. Visible is a deepened mixed layer established by an evaporatively driven convective overturning characteristic for the North-east Monsoon. Salinity in the deeper portion of this layer was in the region of 36.55 ppm.

During the Spring Inter-monsoon, the mixed layer was much less pronounced. A relaxation and subsequent collapse of the East Arabian Current has favored the formation of layered structures, which, in the given case, was reflected by vertical distribution of salinity (Fig. 3). The South-west Monsoon is notorious for its wind-driven coastal upwelling, shallow mixed layer, and subsequent low temperatures in the seasonal thermocline entrained from beneath. For instance, temperature was 21 °C at a 50 m depth, versus 21.5 and 23.5 °C during the Spring Inter-monsoon and North-east Monsoon periods.

Mesoscale variability contributed to the vertical thermo-haline structure as well. Cyclonic and anticyclonic eddies were observed across the shelf throughout the year (Fig. 4). A 3-year weekly animation of the sea surface height anomalies (with a fragment exemplified by Fig. 4) has pointed out three major types of eddies observed in the western Arabian Sea.

Fig. 4
figure 4

Maps of sea surface height anomalies (in cm) featuring the South-west Monsoon season. Left to right 1 August, 2008, and 15 September, 2008

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Numerous eddies move from the Arabian Sea interior westward toward the Omani shelf, throughout the entire year. During the North-east Monsoon, eddies in the western Arabian Sea were poorly developed and the sea surface height anomalies associated with eddies were quite weak. These eddies were observed throughout the Spring Inter-monsoon season as well. During the South-west Monsoon, parts of eddies were generated by the East Arabian Current and its confluence with the current headed out from the Gulf of Oman. In terms of kinetic energy, these are the most powerful eddies in this region. Some of them moved southward when the confluence of currents collapsed, approaching the Fall Inter-monsoon season.

Footprints of monsoon and inter-monsoon periods were pronounced in the chlorophyll-a concentration remotely sensed by the MODIS scanner (Fig. 5). The seasonality of chlorophyll changes was pronounced over shelf waters, but most clearly it was observed over the open sea regions. During the South-west Monsoon, shelf concentrations exceeded the Spring Inter-monsoon period nearly fourfold.

Fig. 5
figure 5

Seasonal changes of the chlorophyll-a concentration in the western Arabian Sea (including the Omani shelf). The vertical color bar stands for the chlorophyll-a concentration (mg m−3). From left to right North-east Monsoon (January–February, 2008), Spring Inter-monsoon (April–May, 2008), and South-west Monsoon (August–September, 2008). White zones in the right figure stand for a cloud mask

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In analyzing spatial and seasonal distribution of zooplankton, we excluded samples collected at night, in order to eliminate the impact of diel vertical migrations, which could cause from a two- to a fivefold increase of zooplankton abundance and biomass (Goswami and Shrivastava 1996; Luo et al. 2000; Smith et al. 1998). Only samples collected during day time (from 6 am to 6 pm) were used to construct the maps. This procedure has limited our subsequent assessments of spatial distribution, making them statistically reliable for the Spring Inter-monsoon and the South-west Monsoon periods only (Fig. 6).

Fig. 6
figure 6

Spatial distribution of zooplankton biomass during Spring Inter-monsoon (left figure) and South-west Monsoon periods

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Maps revealed the biomass distributed mosaically over the shelf area during both seasons. Local maxima with values of approximately 1400–2000 mg m−3 were observed across the shelf and near the shelf edge during both monsoon periods. No seasonal changes were pronounced, regarding the total zooplankton biomass. The mean seasonal values were 689, 723, 543, and 619 mg m−3 for the North-east Monsoon, Spring Inter-monsoon, South-west Monsoon, and Fall Inter-monsoon periods (Table 2). No statistical differences among mean biomass values were observed since the variation was large, which is reflected by the standard deviations.

Table 2 Some basic characteristics of the Omani shelf (2008)
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In spatial distribution, the variance-to-mean ratio has been used as the spatial heterogeneity index (Okubo 1980; Piontkovski and Melnik 2006). In the present study, the ratio was treated as a simple way to assess spatial heterogeneity of zooplankton biomass distribution. As far as the Omani shelf waters are concerned, patchiness in biomass distribution was maximal during the South-west Monsoon (Table 2).

An absent seasonality on the level of total zooplankton biomass was accompanied by a relatively stable species composition of the dominant (by abundance) groups—copepods; 40 species were found during the North-east Monsoon, 38 species during the Spring Inter-monsoon, and 34 species were present in the South-west Monsoon. Of those, 11 species (about 30 %) were present throughout the year (Table 3).

Table 3 List of the copepod species found in samples collected during the North-east Monsoon (NEM), Spring Inter-monsoon (SIM), and the South-west Monsoon (SWM)
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As for the groups of dominant zooplankton species (including copepods), the composition changed throughout the seasons. In the North-east Monsoon, the top five dominant groups were represented by families Oikopleuridae, Sagitta, and copepod species Cosmocalanus darwinii, Nannocalanus minor, and Euchaeta sp., which comprised 15, 10, 10, 5, and 10 % of the total zooplankton abundance, respectively.

In the Spring Inter-monsoon season, fish eggs, decapod larvae, and females of the copepod Centropages tenuiremis dominated the total abundance of zooplankton, and contributed 8 % to total numbers. In the South-west Monsoon, the zooplankton community was dominated by c4 and c5 developmental stages of the copepod Calanoides carinatus s.f., followed by Centropages tenuiremis and Oikopleuridae. C. carinatus s.f. comprising 51 % of the total zooplankton abundance. The other relatively abundant copepod species was Rhincalanus nasutus—with a maximal total prosome length of about 3.5 mm (Table 4).

Table 4 List of the most abundant copepod species on the Omani shelf
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The dominant group exhibited its presence all across the shelf, although the abundance of c4 and c5 copepodite stages of Calanoides carinatus s.f., varied markedly, from 19 to ~6800 ind. m−3 (Fig. 7). In comparison to the North-east Monsoon and Spring Inter-monsoon seasons, the South-west Monsoon was notorious for the dominance of the late copepodite stages and adults of Calanoides carinatus s.f., Centropages tenuiremis, and Rhincalanus nasutus in samples.

Fig. 7
figure 7

Spatial distribution of the abundance of Calanoides carinatus s.f. during the South-west Monsoon

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In order to analyze seasonal changes in the size structure of the entire zooplankton community, organisms were distributed across 16 size classes with the resolution of 0.4 mm. The medians of these classes were used to approximate size distributions (Fig. 8). No prominent changes were observed over seasons. The group with the mean size of 1.8 mm was the dominant one throughout all three seasons. Overall, the community of the North-east Monsoon was characterized by a broad spectrum, whereas the spectrum of the South-west Monsoon community was narrow. The contribution of the dominant group increased, from 28 % during the North-east Monsoon to 59 % during the South-west Monsoon. The twofold increase was driven by the appearance of Calanoides carinatus s.f. No statistical differences were observed among seasons change in the organisms’ mean size. Intra-seasonal variation in the mean size was large, which is reflected in the range of standard deviation (Table 2).

Fig. 8
figure 8

Size structure of zooplankton community over seasons. The abundance of size groups is shown by % of the total zooplankton abundance. NEM North-east Monsoon, SIM spring inter-monsoon, and SWM South-west Monsoon

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Discussion

Seasonal surveys of the zooplankton community across the Omani shelf have enabled us to characterize it as highly productive, with the mean mesozooplankton biomass varying from 543 to 723 mg m−3 throughout the seasonal cycle. These values exceeded the average biomass of the open Arabian Sea regions by three times, which was in a range of 100–200 mg m−3 according to the map of the International Indian Ocean Expedition (Bogorov et al. 1968; Prasad 1968).

Processing of samples has allowed us to identify three general spatial–temporal patterns: (1) the dominance of copepods in the total zooplankton abundance over the shelf waters, (2) the absence of seasonal changes in the level of total zooplankton biomass, and (3) the absence of seasonal changes in the size structure of the zooplankton community.

A leading contribution of copepods to the total abundance of zooplankton has been reported for various regions of the Arabian Sea (Padmavati et al. 1998; Smith and Madhupratap 2005) including Omani coastal waters (Piontkovski et al. 2013). This taxonomic group dominates the zooplankton abundance regardless of seasons.

As far as the seasonality of mesozooplankton biomass is concerned, published data are controversial. The “paradox” of zooplankton biomass reported for the western and eastern Arabian Sea in the early 1990’s (Baars 1999; Madhupratap et al. 1992, 1996) was challenged by subsequent investigators stressing the presence of seasonality (Jyothibabu et al. 2010).

On the level of abundance, lack of seasonal changes of copepod abundance was reported for the central and eastern Arabian Sea (Madhupratap et al. 1996). Nonetheless, it was denoted that the North-east Monsoon season “is always characterized by an increase in the abundance of the cyclopoid copepods, particularly Oithona species, regardless of location in the Arabian Sea” (Smith and Madhupratap 2005). We have not observed this phenomenon, presumably because of the coarse mesh size used; the Oithona species were extremely rare in winter samples, in which females of Oithona plumifera were observed.

Thangaraja et al. (2011), who analyzed the total zooplankton biomass collected by a 200 µm net across the Omani shelf, have reported a 1.8-fold increase during the North-east Monsoon in comparison to the Fall Inter-monsoon period.

In 1994–1996, the absolute maximum in zooplankton biomass was observed during the South-west Monsoon, in the area of coastal upwelling (Smith et al. 1998). The most abundant copepod species in the upwelling area in the upper 25 m layer were the small-bodied copepods Paracalanus aculeatus, Paracalanus denudatus, and Parvocalanus dubia. Four species (P. denudatus, P. dubia, P. aculeatus and Acartia longicornis) accounted for 36 % of the total abundance. With two other species added (Subeucalanus crassus and Calanoides carinatus s.f.), the group accounted for 37 % of total abundance (Smith and Madhupratap 2005). In our case, the group accounting for a major part of total abundance was notoriously different (Table 3). However, the mesh size used in our studies was larger (500 vs 150 µm), which shifted size characteristics and species composition within the community.

During the 1994–1995 cruises, high-frequency acoustical measurements carried out off the Omani shelf pointed out the lowest zooplankton biovolumes during the summer South-West Monsoon, intermediated during fall inter-monsoon, and the highest during the winter North-east Monsoon (Pieper et al. 2001).

The UK “Arabesque” expedition sampled mesozooplankton during and after the 1994 South-west Monsoon (Stelfox et al. 1999), but almost all their “zooplankton stations” (1 out of 8) were outside the shelf area, in which the zooplankton biomass showed a decline from the North-east Monsoon to the fall inter-monsoon period.

One of the factors contributing to seasonal changes and heterogeneous distribution of zooplankton biomass should be a trophic pressure imposed by myctophids. These fishes actively ingest zooplankton, in particular at night when myctophids migrate to upper layers from the deep. Fish trawls and echo-soundings carried out during five seasonal cruises have implied dense layers of myctophids, 20–40 m thick, at about a 200–450 m depth, extending offshore from the shelf during the day and ascending to the upper layer at night, along the shelf edge. The myctophid biomass varied gradually over seasons and was composed mainly of Benthosema pterotum. For instance in the Ras al Hadd region, total myctophid catches accounted for 155 t km−2 during the Spring Inter-monsoon, with a subsequent increase of up to 1.2 M t km−2 by the end of the South-west Monsoon (Devine and Macaulay 2009). Interestingly, these huge changes did not induce an immediate reduction of zooplankton biomass in summer, although the mean value was minimal during the subsequent Fall Inter-monsoon season (Table 2).

On the species level, the most striking feature about seasonal changes in the zooplankton community was the massive appearance of Calanoides carinatus s.f. in the upper mixed layer, to which the population migrated in September, ascending from the depth of about 400 m. This species ingests predominantly diatoms in upwelling areas of the western Indian Ocean (Smith 2001). Interestingly, the appearance of Calanoides carinatus s.f. does not induce prominent seasonal changes in the total zooplankton biomass (Table 2).

We do not have the phytoplankton samples collected at the same place and time as the zooplankton sampling, so remotely sensed chlorophyll-a concentration was the only source used to estimate the magnitude of phytoplankton biomass change over seasons. The chlorophyll maps implied a fairly high biomass in all seasons. A peculiarity of 2008, which was unusual in many aspects including the distortion of a common well-developed seasonal cycle of chlorophyll-a, was the appearance of a massive harmful algal bloom of Cochlodinium polykrikoides during the Fall inter-monsoon, which lasted until spring-2009 (Richlen et al. 2010; Al-Azri et al. 2014).

In terms of spatial distribution, our data point out that the population of Calanoides carinatus s.f. occupies the whole shelf area—from Salalah to Ras al Hadd, although the spatial pattern has exhibited a prominent heterogeneity of biomass distribution—the feature reported by the previous survey carried out in August-1995, when the threefold variance of the dry weight of the biomass was reported along the southern part of the Omani shelf (Hitchcock et al. 2002).

Once the population of Calanoides carinatus s.f. occupies shelf waters, the question is how it gets there (over the continental slope, to depths less than 200 m), if the core of the population is located seaward, in oceanic waters, at the depth of 400 m? At least two aspects of the on-shelf advection could be proposed; the first one is transport by the East Arabian Current from the south. The second one is transport by cyclonic and anticyclonic eddies induced by Rossby waves propagating westward toward the Omani coast (Chelton et al. 2007). In the western Arabian Sea, spatial heterogeneity of zooplankton distribution could be largely explained as being caused by eddies and the mesoscale frontal zones between them (Hitchcock et al. 2002; Piontkovski and Melnik 2006).

On the scale of the Arabian Sea, a statistical relationship between the available potential energy of an eddy field and spatial heterogeneity of zooplankton biomass was reported (Piontkovski et al. 1995). The Omani shelf is a small part, but there, mesoscale eddies are common elements of a regional circulation (Flagg and Kim 1998; Piontkovski and Al-Jufaili 2013; Smith et al. 1991). Eddies entering Omani shelf waters from the central Arabian Sea have been the subject of a specialized expedition aimed at studying the role of eddies in the structure and functioning of the pelagic ecosystem of the western Arabian Sea (Piontkovski and Banse 2006). Zooplankton were collected in the upper 100 m layer at 109 stations in February–April 1990. Biomass maxima usually occurred at the edges of eddies and in frontal zones. The difference between biomass in these maxima was in a region of two- to fourfold.

The variance-to-mean ratio pointed out that zooplankton biomass possessed the most heterogeneous distribution throughout the shelf during the South-west Monsoon period (Table 2). This is the season when eddies are most common over a seasonal cycle of their occurrence in the western Arabian Sea (Piontkovski and Al-Jufaili 2013).

Conclusion

In 2007–2008, the Omani shelf was populated by a highly productive epipelagic plankton community. The chlorophyll-a concentration was high throughout a seasonal cycle and so was the mesozooplankton biomass, values of which nearly threefold exceeded the average biomass of the open Arabian Sea regions. Spatial distribution of zooplankton biomass over shelf waters was highly heterogeneous. The biomass and size structure of the zooplankton community did not exhibit prominent seasonal changes. However, spatial distribution of the zooplankton biomass throughout the shelf was most heterogeneous during the South-west monsoon season.

On the species level, the most striking feature in seasonal changes of the zooplankton community was the massive appearance of the copepod Calanoides carinatus s.f. in shelf waters, to which the population migrated in September. The population, ascending to upper layers during its ontogenetic migration, has occupied the entire Omani shelf area from Salalah to Ras al Hadd.